Association of Rex-1 to target genes supports its interaction with Polycomb function

Stem Cell Research

Volumn 7, Issue 1, 2011, Pages 1-16

  Garcia Tunon I ^c,e   Guallar, D ^c   Alonso Martin, S ^a,f   Benito, A A ^c   Benitez Lazaro A ^c   Perez Palacios R ^c   Muniesa, P ^d   Climent, M ^d   Sanchez M ^a   Vidal, M ^a   Schoorlemmer, J ^a,b,c  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b FUNDACIÓN ARAID   (Spain)

^c INSTITUTO DE INVESTIGACIÓN SANITARIA ARAGÓN IIS ARAGÓN   (Spain)

^d UNIVERSIDAD DE ZARAGOZA   (Spain)

^e HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN; PROTEIN REX 1; REX PROTEIN; TRANSCRIPTION FACTOR YY1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE CONTROL; GENE INTERACTION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HYPOTHESIS; INNER CELL MASS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION; GENES, HOMEOBOX; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; PREGNANCY; RABBITS; REPRESSOR PROTEINS; TRANSFECTION;

EID: 79956348828     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2011.02.005     Document Type: Article

References (81)

1. Affar E.B., Gay F., Shi Y., Liu H., Huarte M., Wu S., Collins T., Li E. Essential dosage-dependent functions of the transcription factor yin yang 1 in late embryonic development and cell cycle progression. Mol. Cell. Biol. 2006, 26:3565-3581.
2. Alkema M.J., Bronk M., Verhoeven E., Otte A., van 't Veer L.J., Berns A., van Lohuizen M. Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev. 1997, 11:226-240.
3. Aubert J., Dunstan H., Chambers I., Smith A. Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat. Biotechnol. 2002, 20:1240-1245.
4. Avilion A., Nicolis S., Pevny L., Perez L., Vivian N., Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003, 17:126-140.
5. Azuara V., Perry P., Sauer S., Spivakov M., Jørgensen H., John R., Gouti M., Casanova M., Warnes G., Merkenschlager M., Fisher A. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 2006, 8:532-538.
6. Bernstein B., Mikkelsen T., Xie X., Kamal M., Huebert D., Cuff J., Fry B., Meissner A., Wernig M., Plath K., Jaenisch R., Wagschal A., Feil R., Schreiber S., Lander E. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
7. Boyer L., Mathur D., Jaenisch R. Molecular control of pluripotency. Curr. Opin. Genet. Dev. 2006, 16:455-462.
8. Boyer L., Plath K., Zeitlinger J., Brambrink T., Medeiros L., Lee T., Levine S., Wernig M., Tajonar A., Ray M., Bell G., Otte A., Vidal M., Gifford D., Young R., Jaenisch R. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
9. Braun P., Tasan M., Dreze M., Barrios-Rodiles M., Lemmens I., Yu H., Sahalie J., Murray R., Roncari L., de Smet A., Venkatesan K., Rual J., Vandenhaute J., Cusick M., Pawson T., Hill D., Tavernier J., Wrana J., Roth F., Vidal M. An experimentally derived confidence score for binary protein-protein interactions. Nat. Methods 2009, 6:91-97.
10. Brivanlou A., Gage F., Jaenisch R., Jessell T., Melton D., Rossant J. Stem cells. Setting standards for human embryonic stem cells. Science 2003, 300:913-916.
11. Brons I., Smithers L., Trotter M., Rugg-Gunn P., Sun B., Chuva de Sousa Lopes S., Howlett S., Clarkson A., Ahrlund-Richter L., Pedersen R., Vallier L. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007, 448:191-195.
12. Brown J., Mucci D., Whiteley M., Dirksen M., Kassis J. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol. Cell 1998, 1:1057-1064.
13. Cao R., Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 2004, 14:155-164.
14. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
15. Chan E., Ratanasirintrawoot S., Park I., Manos P., Loh Y., Huo H., Miller J., Hartung O., Rho J., Ince T., Daley G., Schlaeger T. Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat. Biotechnol. 2009, 27:1033-1037.
16. del Mar Lorente M., Marcos-Gutiérrez C., Pérez C., Schoorlemmer J., Ramírez A., Magin T., Vidal M. Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice. Development 2000, 127:5093-5100.
17. Donohoe M., Zhang X., McGinnis L., Biggers J., Li E., Shi Y. Targeted disruption of mouse Yin Yang 1 transcription factor results in peri-implantation lethality. Mol. Cell. Biol. 1999, 19:7237-7244.
18. Endoh M., Endo T., Endoh T., Fujimura Y., Ohara O., Toyoda T., Otte A., Okano M., Brockdorff N., Vidal M., Koseki H. Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 2008, 135:1513-1524.
19. García E., Marcos-Gutiérrez C., del Mar Lorente M., Moreno J., Vidal M. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1. EMBO J. 1999, 18:3404-3418.
20. Gearhart M., Corcoran C., Wamstad J., Bardwell V. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol. Cell. Biol. 2006, 26:6880-6889.
21. Gordon S., Akopyan G., Garban H., Bonavida B. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 2006, 25:1125-1142.
22. Hamatani T., Carter M., Sharov A., Ko M. Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 2004, 6:117-131.
23. Harlow E., Lane D. Using Antibodies: A Laboratory Manual 1998, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
24. Hosler B., LaRosa G., Grippo J., Gudas L. Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol. Cell. Biol. 1989, 9:5623-5629.
25. Hu G., Kim J., Xu Q., Leng Y., Orkin S., Elledge S. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 2009, 23:837-848.
26. Jeong Y., Choi H., Shin H., Cui X., Kim N., Gerton G., Jun J. Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. Mol. Reprod. Dev. 2005, 71:284-289.
27. Jiang Y., Jahagirdar B., Reinhardt R., Schwartz R., Keene C., Ortiz-Gonzalez X., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W., Largaespada D., Verfaillie C. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
28. Kalenik J., Chen D., Bradley M., Chen S., Lee T. Yeast two-hybrid cloning of a novel zinc finger protein that interacts with the multifunctional transcription factor YY1. Nucleic Acids Res. 1997, 25:843-849.
29. Karlmark K., Freilinger A., Marton E., Rosner M., Lubec G., Hengstschläger M. Activation of ectopic Oct-4 and Rex-1 promoters in human amniotic fluid cells. Int. J. Mol. Med. 2005, 16:987-992.
30. Kim J., Hinz A., Bergmann A., Huang J., Ovcharenko I., Stubbs L., Kim J. Identification of clustered YY1 binding sites in imprinting control regions. Genome Res. 2006, 16:901-911.
31. Kim S., Paylor S., Magnuson T., Schumacher A. Juxtaposed Polycomb complexes co-regulate vertebral identity. Development 2006, 133:4957-4968.
32. Kim J., Faulk C., Kim J. Retroposition and evolution of the DNA-binding motifs of YY1, YY2 and REX1. Nucleic Acids Res. 2007, 35:3442-3452.
33. Kim J., Chu J., Shen X., Wang J., Orkin S. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008, 132:1049-1061.
34. Klymenko T., Papp B., Fischle W., Köcher T., Schelder M., Fritsch C., Wild B., Wilm M., Müller J. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 2006, 20:1110-1122.
35. Ku M., Koche R., Rheinbay E., Mendenhall E., Endoh M., Mikkelsen T., Presser A., Nusbaum C., Xie X., Chi A., Adli M., Kasif S., Ptaszek L., Cowan C., Lander E., Koseki H., Bernstein B. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008, 4:e1000242.
36. Li G., Margueron R., Ku M., Chambon P., Bernstein B., Reinberg D. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 2010, 24:368-380.
37. Loh Y., Wu Q., Chew J., Vega V., Zhang W., Chen X., Bourque G., George J., Leong B., Liu J., Wong K., Sung K., Lee C., Zhao X., Chiu K., Lipovich L., Kuznetsov V., Robson P., Stanton L., Wei C., Ruan Y., Lim B., Ng H. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 2006, 38:431-440.
38. Mak W., Baxter J., Silva J., Newall A., Otte A., Brockdorff N. Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr. Biol. 2002, 12:1016-1020.
39. Masui S., Ohtsuka S., Yagi R., Takahashi K., Ko M., Niwa H. Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells. BMC Dev. Biol. 2008, 8:45.
40. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
41. Mohd-Sarip A., Cléard F., Mishra R., Karch F., Verrijzer C. Synergistic recognition of an epigenetic DNA element by Pleiohomeotic and a Polycomb core complex. Genes Dev. 2005, 19:1755-1760.
42. Müller J., Verrijzer P. Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr. Opin. Genet. Dev. 2009, 19:150-158.
43. Nagy A., Gertsenstein M., Vintersten K., Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
44. Navarro P., Oldfield A., Legoupi J., Festuccia N., Dubois A., Attia M., Schoorlemmer J., Rougeulle C., Chambers I., Avner P. Molecular coupling of Tsix regulation and pluripotency. Nature 2010, 468:457-460.
45. Nichols J., Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4:487-492.
46. Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Schöler H., Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391.
47. Niwa H., Burdon T., Chambers I., Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 1998, 12:2048-2060.
48. Okita K., Ichisaka T., Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007, 448:313-317.
49. Palmieri S., Payne J., Stiles C., Biggers J., Mercola M. Expression of mouse PDGF-A and PDGF alpha-receptor genes during pre- and post-implantation development: evidence for a developmental shift from an autocrine to a paracrine mode of action. Mech. Dev. 1992, 39:181-191.
50. Pasini D., Cloos P., Walfridsson J., Olsson L., Bukowski J., Johansen J., Bak M., Tommerup N., Rappsilber J., Helin K. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 2010, 464:306-310.
51. Pietersen A., van Lohuizen M. Stem cell regulation by polycomb repressors: postponing commitment. Curr. Opin. Cell Biol. 2008, 20:201-207.
52. Ratnam S., Mertineit C., Ding F., Howell C., Clarke H., Bestor T., Chaillet J., Trasler J. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev. Biol. 2002, 245:304-314.
53. Rogers M., Hosler B., Gudas L. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 1991, 113:815-824.
54. Rossant J. Stem cells and lineage development in the mammalian blastocyst. Reprod. Fertil. Dev. 2007, 19:111-118.
55. Ruddock-D'Cruz N., Prashadkumar S., Wilson K., Heffernan C., Cooney M., French A., Jans D., Verma P., Holland M. Dynamic changes in localization of Chromobox (Cbx) family members during the maternal to embryonic transition. Mol Reprod Dev 2008, 75:477-488.
56. Rugg-Gunn P., Cox B., Ralston A., Rossant J. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc. Natl Acad. Sci. U.S.A. 2010, 107:10783-10790.
57. Sánchez C., Sánchez I., Demmers J., Rodriguez P., Strouboulis J., Vidal M. Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol. Cell. Proteomics 2007, 6:820-834.
58. Satijn D., Hamer K., den Blaauwen J., Otte A. The polycomb group protein EED interacts with YY1, and both proteins induce neural tissue in Xenopus embryos. Mol. Cell. Biol. 2001, 21:1360-1369.
59. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
60. Schwartz Y., Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 2007, 8:9-22.
61. Schlisio S., Halperin T., Vidal M., Nevins J. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. EMBO J. 2002, 21:5775-5786.
62. Schoorlemmer J., Marcos-Gutiérrez C., Were F., Martínez R., García E., Satijn D., Otte A., Vidal M. Ring1A is a transcriptional repressor that interacts with the Polycomb-M33 protein and is expressed at rhombomere boundaries in the mouse hindbrain. EMBO J. 1997, 16:5930-5942.
63. Scotland K., Chen S., Sylvester R., Gudas L. Analysis of Rex1 (zfp42) function in embryonic stem cell differentiation. Dev. Dyn. 2009, 238:1863-1877.
64. Shen X., Kim W., Fujiwara Y., Simon M., Liu Y., Mysliwiec M., Yuan G., Lee Y., Orkin S. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 2009, 139:1303-1314.
65. Simon J., Kingston R. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 2009, 10:697-708.
66. Smith A. The battlefield of pluripotency. Cell 2005, 123:757-760.
67. Spanopoulou E., Zaitseva F., Wang F., Santagata S., Baltimore D., Panayotou G. The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 1996, 87:263-276.
68. Spivakov M., Fisher A. Epigenetic signatures of stem-cell identity. Nat. Rev. Genet. 2007, 8:263-271.
69. Surface L., Thornton S., Boyer L. Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 2010, 7:288-298.
70. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
71. Tanaka S., Kunath T., Hadjantonakis A., Nagy A., Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282:2072-2075.
72. Tesar P., Chenoweth J., Brook F., Davies T., Evans E., Mack D., Gardner R., McKay R. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448:196-199.
73. Torres-Padilla M., Bannister A., Hurd P., Kouzarides T., Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 2006, 50:455-461.
74. Toyooka Y., Shimosato D., Murakami K., Takahashi K., Niwa H. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 2008, 135:909-918.
75. Umlauf D., Goto Y., Cao R., Cerqueira F., Wagschal A., Zhang Y., Feil R. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 2004, 36:1296-1300.
76. Wang L., Brown J., Cao R., Zhang Y., Kassis J., Jones R. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 2004, 14:637-646.
77. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R., Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431:873-878.
78. Wang J., Rao S., Chu J., Shen X., Levasseur D.N., Theunissen T.W., Orkin S.H. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006, 444:364-368.
79. Woo C., Kharchenko P., Daheron L., Park P., Kingston R. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 2010, 140:99-110.
80. Xu J., Sylvester R., Tighe A., Chen S., Gudas L. Transcriptional activation of the suppressor of cytokine signaling-3 (SOCS-3) gene via STAT3 is increased in F9 REX1 (ZFP-42) knockout teratocarcinoma stem cells relative to wild-type cells. J. Mol. Biol. 2008, 377:28-46.
81. Zhang J., Gao W., Yang H., Zhang B., Zhu Z., Xue Y. Screening for genes essential for mouse embryonic stem cell self-renewal using a subtractive RNA interference library. Stem Cells 2006, 24:2661-2668.